In the operation of the forward osmosis (FO) process, biofouling of the membrane is a potentially serious problem. Development of an FO membrane with antibacterial properties could contribute to a reduction in biofouling. In this study, quaternary ammonium cation (QAC), a widely used biocidal material, was conjugated with a silane coupling agent (3-(trimethoxysilyl)-propyldimethyloctadecyl ammonium chloride) and used to modify an FO membrane to confer antibacterial properties. Fourier transform infrared spectroscopy (FT-IR) demonstrated that the conjugated QAC was successfully immobilized on the FO membrane via covalent bonding. Bacterial viability on the QAC-modified membrane was confirmed via colony count method and visualized via bacterial viability assay. The QAC membrane decreased the viability of Escherichia coli to 62% and Staphylococcus aureus to 77% versus the control membrane. Inhibition of biofilm formation on the QAC modified membrane was confirmed via anti-biofilm tests using the drip-flow reactor and FO unit, resulting in 64% and 68% inhibition in the QAC-modified membrane against the control membrane, respectively. The results demonstrate the effectiveness of the modified membrane in reducing bacterial viability and inhibiting biofilm formation, indicating the potential of QAC-modified membranes to decrease operation costs incurred by biofouling.

INTRODUCTION

Forward osmosis (FO) is a method for separating clean water from a feed solution by drawing the water from the feed to a high solute concentration draw solution via a semi-permeable membrane. This highlights the FO process operation using naturally occurring osmosis and contrasts with the high hydraulic pressure needed in the reverse osmosis (RO) process. In principle, no hydraulic pressure is required to pass water across the membrane in FO processes. In addition to the low energy requirement, the advantages of the FO process are many: low fouling propensity, easy cleaning, high salt rejection, and high water flux (Zhao et al. 2012). Thus, FO processes have the potential to treat wastewater, concentrate landfill leachate, reclaim wastewater for drinking water, and generate power (Cath et al. 2006; Zhao et al. 2012). However, several challenges need to be overcome for widespread use of the FO process; these include concentration polarization, membrane fouling, reverse solute diffusion, membrane development, and draw solute (Zhao et al. 2012).

Like other membrane filtration technologies, FO processes tend to be fouled during operation. Although FO processes have shown low membrane fouling due to low hydraulic pressure operation, membrane fouling appears to be an unavoidable phenomenon. In particular, when FO processes operate in conjunction with bioreactors, or osmotic membrane bioreactors (OMBR), membrane fouling of the active layer occurs via microorganisms from the activated sludge, i.e., biofouling (Cornelissen et al. 2008; Yoon et al. 2013). When microorganisms attach on biotic or abiotic surfaces, they tend to form biofilms. Microorganisms in biofilms are encased in a self-secreted extracellular polymeric substance and are notoriously difficult to remove (Sauer et al. 2002; Cosenza et al. 2013). Biofouling reduces water flux across the membrane, increases operating pressure, reduces membrane life, and ultimately burdens operating costs. Thus, strategies to reduce biofouling in FO processes are needed, especially in OMBR processes.

Strategies in reducing biofouling potential in OMBR processes include optimization of operating conditions and development of anti-biofouling membranes. Optimization of operating conditions can be achieved by modulating solids retention time, dissolved oxygen concentration, activated sludge concentration, water flux, etc. Development of anti-biofouling membranes includes modification of surface chemistry and topology and the immobilization of anti-microbial materials. Immobilization of anti-microbial materials (e.g., nano-particles and biocides) may directly influence the viability of microorganisms attached to the membrane surface. Of such anti-microbial materials, quaternary ammonium cation (QAC) is a compound consisting of a monovalent nitrogen cation to which four alkyl (or aryl) groups are bonded . QAC has been shown to be effective on various microorganisms, such as bacteria, fungi, algae, and viruses (Ahlström et al. 1995). One of the mechanisms for killing microorganisms is based on the electrostatic attraction of negatively-charged microorganisms to positively charged QAC (McDonnell & Russell 1999). The microorganisms–QAC complexes result in the disruption of the microbial cell wall, ultimately killing the microorganism. The biocidal mechanism suggests the applicability of QAC to anti-microbial surfaces. In practice, QAC has been applied to provide anti-bacterial properties on various surfaces such as silicon rubber (Gottenbos et al. 2002), textiles (Gao & Cranston 2008; Simoncic & Tomsic 2010), cotton–polyester fabric (Murray et al. 1988), catheters, etc. Recently, Zhang et al. (2014) reported that modification of an RO membrane with QAC was effective in killing bacteria and retarding water flux decrease after biofouling. However, they did not evaluate the effect of QAC immobilization on biofilm formation, which is the major cause of membrane biofouling (Herzberg & Elimelech 2007). Furthermore, they applied the QAC-modified membrane to the RO process and not to the FO process. Thus, whether or not QAC immobilization onto membrane surfaces effectively reduces biofouling in the FO processes is a question yet to be answered.

Therefore, the primary objectives of this study were to immobilize QAC on an FO membrane to evaluate the anti-bacterial and anti-biofilm effects of the QAC-modified membrane. For QAC immobilization, QAC was conjugated with a silane coupling agent to facilitate covalent bonding between QAC and the FO membrane active layer. For the evaluation of the anti-bacterial and anti-biofilm properties of the modified membrane, colony count method, viability assay, and anti-biofilm tests were employed on model Gram-negative and Gram-positive bacteria.

MATERIALS and METHODS

QAC immobilization

The FO membrane used in this study was a composite membrane consisting of a polysulfone support layer and a polyamide active skin layer obtained from Toray Chemical Korea, Inc. (Seoul, Korea). QAC conjugated with a silane coupling agent, 3-(trimethoxysilyl)-propyldimethyloctadecyl ammonium chloride (Gelest, Inc., Morrisville, PA, USA), was immobilized via covalent bonding onto the polyamide active skin layer of the FO membrane. QAC immobilization was performed via the following steps: (i) the FO membrane was plasma treated under a 0.2 m Torr vacuum for 1 min, allowing the N–H bond in the amide group to be converted to an N radical (Kang & Cao 2012); (ii) QAC solution, prepared by mixing 47.5 ml ethanol, 2.5 ml deionized (DI) water, 2.5 ml acetic acid, and 1.0 ml QAC, was slowly stirred for 3–5 min to allow hydrolysis and condensation; (iii) plasma-treated FO membrane was dipped into slow-stirred QAC solution for 1–2 min to bond the N radical with the silane coupling agent, which conjugated with QAC; (iv) the membrane was dried for 48 h in a 50 °C oven to induce bond formation; and finally (v) the QAC-immobilized FO membrane was washed with DI water several times to remove non-immobilized QAC from the FO membrane surface. The conditions for QAC immobilization onto the FO membrane were based on the protocol suggested by the supplier of the silane coupling agent (Gelest, Inc.).

Fourier transform infrared spectroscopy (FT-IR) analysis

FT-IR spectroscopy analysis was conducted to characterize the surface chemical structure for the FO membranes before and after QAC modification using the Spectrum 2000 FT-IR (Perkin-Elmer, Waltham, MA, USA). An attenuated total reflectance (ATR) mode using a mercury cadmium telluride detector was applied. Wavelengths were set at 600–4,000 cm−1 at a resolution of 0.5 cm−1 with 256 scans.

Bacterial strains and their culture conditions

In this study, two bacterial species were used to test viability, and one species was used to test biofilm inhibition. Specifically, Escherichia coli strain K-12, representing a model Gram-negative bacterium, and Staphylococcus aureus strain ATCC6538, representing a model Gram-positive bacterium, were used to confirm bacteria viability on QAC-modified membrane. Pseudomonas aeruginosa strain PA14, as a model biofilm-forming bacterium, was used to confirm the biofilm-inhibition property of QAC-modified membrane. Each bacterium was incubated overnight in 5 ml Luria-Bertani (LB) broth at 37 °C in a shaking incubator 1 day prior to each experiment. During the bacteria viability test, bacteria were washed using sterilized 0.9% NaCl solution to control bacterial growth. During the biofilm inhibition test, bacteria were incubated in LB broth to form biofilms onto FO membrane.

Colony count

Escherichia coli and S. aureus were incubated overnight in 5 ml of LB broth at 37 °C in a shaking incubator. One milliliter of bacterial culture was centrifuged for 3 min at 14,400 rpm. The pellet was washed with 1 ml of sterilized 0.9% NaCl solution, then centrifuged and washed three more times. The FO membrane without treatment (control) and the membrane immobilized with QAC (QAC-modified) was cut using sterilized scissors into 1 × 1 cm2, then 4 cuvettes were set up with a single square in each. Prepared S. aureus and E. coli was diluted 10 times and 500 μl of the final dilution was aliquoted into a cuvette. The reaction proceeded at 37 °C for 3 h. Of note, 100 μl of each bacteria culture was diluted 10-fold, 5 times using 900 μl of sterilized 0.9% NaCl solution from 10−2 to 10−6. Then, 100 μl of the dilution was spread onto an LB agar plate (N = 5) and placed in a 37 °C incubator overnight. Finally, the number of colonies was counted to determine the number of viable microorganisms. Thus, the ratio of bacteria viability on the QAC-modified membrane and control membrane was determined.

Bacterial viability assay

In the same manner as the colony count, E. coli were prepared and reacted with the control membrane and the QAC-modified membrane. After 3 h, the bacterial culture was diluted 1/10 with sterilized 0.9% NaCl solution. Diluted bacterial culture was stained using the LIVE/DEAD® BacLight™ bacterial viability kit (Molecular Probes, Eugene, OR, USA) to selectively dye live cells with a green hue and dead cells with red; 3.34 mM SYTO® 9 nucleic acid 3 μl and 20 mM propidium iodide (PI) 3 μl was added into 1 ml of each sample, and the bacteria were stained for 15 min in the dark. After dyeing the cells, the sample was filtered with a 0.2 μm filter. Confocal laser scanning microscopy (CLSM, Carl Zeiss LSM700, Jena, Germany) was used for measuring viable and non-viable microorganisms: ×400 objective lens, enhanced green fluorescent protein (EGFP; green)/PI (red) mode; the settings were average: number = 4, speed = 4, zoom = 2×. CLSM images of each sample were analyzed using Zen 2011 (Carl Zeiss, Oberkochen, Germany). Thus, the bactericidal effect of QAC-modified membrane was visualized.

Anti-biofilm test using the drip-flow reactor

To sterilize, a drip-flow reactor (DFR 110, Biosurface, Bozeman, MT, USA) was washed with alcohol and autoclaved at 121 °C for 15 min (Figure 1). The pump was washed with alcohol for 6 h and then washed with sterilized DI water for 3 h to remove the alcohol from each tube. After preparing the reactor, P. aeruginosa was incubated overnight in 5 ml of LB broth at 37 °C in a shaking incubator. One milliliter of the bacterial culture was added to 99 ml of LB broth for a 1/100 dilution, which again was incubated overnight. Then, 100 ml of the culture was added to 1.9 l of LB broth, making a 1/20 dilution. The final dilution culture was then placed in a 37 °C incubator. The control membrane and QAC-modified membrane was attached to sterilized glass slides, and the slides were inserted into the drip-flow reactor. A small amount of LB broth was then pump-dripped (flow rate of 20 ml/h) onto the slides for 3 days, during which biofilm development occurred. After 3 days, the slides were washed twice with phosphate-buffered saline (PBS, 50 mM NaH2PO4/Na2HPO4, 154 mM NaCl, pH = 7.4) and DI water, respectively. Then, 400 μl of 4′,6-diamidino-2-phenylindole (DAPI; Carl Roth, Karlsruhe, Germany) was added to the slides and left to stain for 20 min in the dark. Afterwards, the slides were washed again with PBS, and the biofilm was analyzed using the Carl Zeiss LSM700 CLSM using the Z-stack function for 3D imaging, and the CLSM images were analyzed with the Zen 2011 program (Carl Zeiss). Thus, biofilm formation on each control and QAC-modified membrane was visualized. In addition, biofilms on each membrane were quantified using image J program (National Institutes of Health, Bethesda, MD, USA).

Figure 1

Schematic diagram of the drip-flow reactor used for biofilm formation.

Figure 1

Schematic diagram of the drip-flow reactor used for biofilm formation.

Anti-biofilm test using the FO unit test

To confirm the biofilm inhibition property of the QAC-modified membrane under FO process conditions, a laboratory-scale FO unit test was performed for both control membrane and QAC-modified membrane. The FO unit used in this experiment is described in a previous publication (Kim et al. 2014). P. aeruginosa culture (optical density (OD) at 595 nm = 0.1) was used as feed solution for the FO unit to form biofilms on the active layer of the FO membrane during operation. Of note, 2 M of NaCl was used as draw solution to separate water from the feed; the FO unit was operated at 25 °C for 15 h at 8.5 cm/s of cross-flow of feed and draw solution.

After operation, each membrane was cut using sterilized scissors into 2 × 2 cm2 and washed twice with PBS solution. Then, each membrane was stained with 0.1% crystal violet for 30 min and washed with DI water for 1 hour with shaking. The dyed membranes were then placed into 10 ml of 100% ethanol and sonicated for 10 min. Finally, the concentration of crystal violet was measured by OD at 545 nm using an iMark micro-plate reader (BioRad, Richmond, CA, USA). In addition, control and QAC-modified membranes were dyed using crystal violet without operation of the FO unit and OD at 545 nm was measured. OD at 545 nm of the biofilm itself was calculated by subtracting the OD at 545 nm of the blank membranes from the OD at 545 nm of the membranes used during operation. Thus, the biofilm itself on each membrane after operation of the FO unit was quantified.

RESULTS and DISCUSSION

Immobilization of QAC

The surface of unmodified (control) and QAC-modified membranes were characterized by FT-IR spectroscopy from 500 to 4,000 cm−1 to confirm covalent bonds between QAC and the polyamide layer of the FO membrane. As shown in Figure 2 (black lines), the unmodified membrane showed characteristic FT-IR spectra of polyamide-based membrane in which amide I (1,671 cm−1) and amide II peaks (1,550 cm−1) were observed. It has been reported that amide I peak is indicative of C = O stretching (largest contribution), C–N stretching, and C–C–N deformation vibration in a secondary amide group (Skrovanek et al. 1985), while the amide II peak arises from N–H in-plane bending, C–N stretching vibration of –CO–NH– group and C–C stretching vibration (Skrovanek et al. 1985). The unmodified membrane also showed peaks originating from the polysulfone support layer at 1,486, 1,503, and 1,584 cm−1 (Freger et al. 2002). The polysulfone peaks represent aromatic in-plane ring bend stretching vibrations.

Figure 2

FT-IR ATR spectra of QAC-modified membrane (gray line) and unmodified membrane (control, black line).

Figure 2

FT-IR ATR spectra of QAC-modified membrane (gray line) and unmodified membrane (control, black line).

Conversely, the spectra of QAC-modified membrane (gray line in Figure 2) were somewhat different from the unmodified membrane. Although the characteristic polysulfone peaks were also observed in the spectra of QAC-modified membrane, QAC signatures and an altered amide I peak were observed. The QAC-modified membrane exhibited characteristic C–H stretching peaks (2,850 and 2,916 cm−1) (Skrovanek et al. 1985; Wang & Griffiths 1985), which were not evident in the unmodified membrane, demonstrating that QAC molecules were present on the surface of the FO membrane. Regarding the amide I peak in the QAC-modified membrane, the wave number shifted from 1,671 to 1,716 cm−1. This could be evidence of a covalent bonding between QAC and the polyamide layer. As shown in Figure 3(a), the carbonyl group (C=O) of the unmodified membrane will be influenced by adjacent hydrogen, which is attached to nitrogen by hydrogen bonding. If hydrogen is substituted with other atoms or groups, the C=O stretching peak will be shifted (i.e., release of the influence of the hydrogen bond) (Kwon & Leckie 2006). It appears that the immobilization process used in this study substituted the hydrogen with QAC (see Figure 3(c)), which resulted in a shift of C=O stretching peak from 1,671 to 1,716 cm−1. In the FT-IR spectra of the QAC-modified membrane, simultaneous observations of QAC signatures and a shift of C=O stretching peak could provide evidence of a successful covalent bond between QAC and the polyamide layer of the FO membrane. Although this study did not evaluate the long-term stability of immobilized QAC onto the FO membrane, it is expected to be stable in the long-term due to binding via covalent bonding rather than physisorption. This speculation is supported by other studies that have dealt with QAC binding onto various surfaces (Vasilev et al. 2009; Charnley et al. 2011).

Figure 3

Schematic diagram showing immobilization of QAC. (a) Amide group of unmodified membrane. (b) N radical formation by plasma treatment. (c) Covalent bond formation between QAC and amide group of membrane.

Figure 3

Schematic diagram showing immobilization of QAC. (a) Amide group of unmodified membrane. (b) N radical formation by plasma treatment. (c) Covalent bond formation between QAC and amide group of membrane.

Bacteria viability

To test whether the modified membrane possesses anti-bacterial properties or not, E. coli and S. aureus were incubated in 0.9% NaCl solution with control and QAC-modified membrane coupons for 3 hours, respectively. Colony numbers were significantly lower in the cultures with the modified membrane for both bacterial strains. Figure 4(a) shows the differences in colony numbers for the cultures with unmodified and QAC-modified membranes. The E. coli colony numbers were 7.5 × 107 ± 0.3 CFU/ml with the unmodified membrane and 1.8 × 107 ± 0.2 CFU/ml with the QAC-modified membrane, respectively (62% reduction). For S. aureus, the colony numbers were 13.0 × 107 ± 2.8 CFU/ml with the unmodified membrane and 4.9 × 107 ± 0.9 CFU/ml with the QAC-modified membrane (77% reduction). Both experiments were conducted in five independent trials and Student's t-test for both experiments showed P < 0.05, indicating the difference as statistically significant. The above results demonstrate that the QAC-modified membrane was effective in killing bacteria within a relatively short period of time (i.e., 3 hours of incubation).

Figure 4

Anti-bacterial property. (a) Comparison of E. coli and S. aureus colony numbers after incubation in LB media with control and QAC-modified membranes. Error bars indicate standard deviations of five measurements. (b) CLSM image of E. coli cells after incubation in LB media with control and QAC-modified membranes. Live and dead E. coli cells are shown in green and red hue, respectively. The full color version of this figure is available online at http://www.iwaponline.com/wst/toc.htm.

Figure 4

Anti-bacterial property. (a) Comparison of E. coli and S. aureus colony numbers after incubation in LB media with control and QAC-modified membranes. Error bars indicate standard deviations of five measurements. (b) CLSM image of E. coli cells after incubation in LB media with control and QAC-modified membranes. Live and dead E. coli cells are shown in green and red hue, respectively. The full color version of this figure is available online at http://www.iwaponline.com/wst/toc.htm.

Although the colony count method could quantify live cells effectively, the method has inherent limitation in analyzing dead bacterial cells. To quantify the dead bacterial cells as well as live bacterial cells, the LIVE/DEAD® BacLight™ bacterial viability kit was used to selectively dye viable and non-viable cells according to hue. Figure 4(b) shows the CLSM images of live and dead E. coli cells indicated by green (dyed by Syto®9 nucleic acid) and red (dyed by PI) hues, respectively. The control membrane image shows a greater proportion of green hue over red (77% green cells). The QAC-modified membrane image, inversely, shows a greater proportion of red hue (72% red cells). This difference in proportion of hue also indicates that the QAC-modified membrane exhibited effective bactericidal activity. A proportion of red hue (23%) was observed on the control CLSM image without a completely green hue. This result is most likely due to natural decay of bacteria (e.g., endogenous decay) instead of the antibacterial effect of the control membrane.

Inhibition of biofilm formation

Biofouling is caused not only by bacterial cells lodged on the membrane but also actual biofilm formation; the latter shows much more resistance to removal and is the major problem concerning biofouling (Herzberg & Elimelech 2007). To test whether or not the modified membrane is also effective in reducing biofilm formation, biofilms were grown on the control and QAC-modified membrane using the drip-flow reactor. Figure 5 shows the three-dimensional CLSM image of biofilms on the control and QAC-modified membrane after a 3-day reaction. The control membrane shows a generally flat biofilm covering the whole membrane with an average height of ∼12 μm. The image for the QAC-modified membrane shows, in contrast, hill-like structures with conspicuously more vacant membrane surface and a shorter average height of 3 μm.

Figure 5

CLSM images of P. aeruginosa biofilms on control and QAC-modified membranes. Biofilm cells were stained with DAPI solution before obtaining images.

Figure 5

CLSM images of P. aeruginosa biofilms on control and QAC-modified membranes. Biofilm cells were stained with DAPI solution before obtaining images.

In addition, the biofilm on each membrane was quantified via image J program. The total pixel area of the control membrane is 3.5 × 105 pixel2 and is 1.3 × 105 pixel2 for the QAC-modified membrane; the area ratio between control and QAC-modified membranes is 2.75. Accordingly, the QAC-modified membrane demonstrated a 64% decrease in biofilm formation compared with the control membrane. These results confirm the QAC-modified membrane's antibacterial property and demonstrates its capacity for inhibiting biofilm formation.

To test the performance of the QAC-modified membrane in the context of the FO process, a laboratory-scale FO unit was set up using both membranes. The FO unit was operated for 15 h, and biofilms were formed on the control and QAC-modified membranes. Biofilms on the control membrane were much more formed than on the QAC-modified membrane. This was evidenced qualitatively by visualization of the membrane at the end of the FO unit operation. In Figure 6(a), the membrane photos show the biofilm formed during the 15 hours of operation. To analyze the biofilm development quantitatively, the OD at 545 nm of both control and modified membranes were measured and found to be 0.185 and 0.060, respectively (Figure 6(b)). Thus, the QAC-modified membrane was found to inhibit 68% of biofilm formation versus the control membrane; this result being nearly identical to that of the drip-flow reactor (64% biofilm inhibition). Both drip-flow reactor and FO unit test results showed that the QAC-modified membrane demonstrated biofilm inhibition during reactor operation. However, it must be noted that although QAC immobilization provided the FO membrane with antibacterial and antibiofilm properties, the modification sacrificed water flux. Initial water flux of the modified and the unmodified FO membranes was 1.6 μm/s and 3.1 μm/s, respectively.

Figure 6

Comparison of biofilm formation between control and QAC-modified membranes after 15 hours of operation. (a) Photos of membrane surfaces after 15 hours of operation. (b) Quantity of biofilm on each membrane via measuring OD at 545 nm. Error bars indicate standard deviations of five measurements.

Figure 6

Comparison of biofilm formation between control and QAC-modified membranes after 15 hours of operation. (a) Photos of membrane surfaces after 15 hours of operation. (b) Quantity of biofilm on each membrane via measuring OD at 545 nm. Error bars indicate standard deviations of five measurements.

CONCLUSIONS

In this study, QAC was covalently immobilized on the FO membrane as confirmed by FT-IR spectroscopy. The colony count method and the live/dead kit tests showed that the QAC-modified membrane possessed antibacterial properties for E. coli and S. aureus bacteria. Anti-biofilm tests for the QAC-modified membrane using the drip-flow reactor and FO unit test demonstrated significant reductions in biofilm-formation by up to two-thirds compared with the control membrane. These results show that the immobilization of QAC on the FO membrane confers bactericidal and biofilm-inhibiting properties to the membrane. The effective reduction of biofilm formation offered by the QAC-modified membrane has the potential to be applied in the FO process to reduce membrane maintenance and overall operation costs via the reduction of biofouling. In addition, the QAC modification may also be applied as a biofouling control in other dimensions of porous membranes such as microfiltration and ultrafiltration membranes.

ACKNOWLEDGEMENTS

We would like to thank Ted Inpyo Hong for proofreading this manuscript. This study was funded by Toray Chemical Korea Inc. and a Korea University grant.

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